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Volume 16, Number 2—February 2010

Associations between Mycobacterium tuberculosis Strains and Phenotypes

Timothy Brown1, Vladyslav Nikolayevskyy1, Preya Velji, and Francis DrobniewskiComments to Author 
Author affiliations: United Kingdom Health Protection Agency, London UK (T. Brown, F. Drobniewski); Queen Mary College, University of London, London (V. Nikolayevskyy, P. Velji, F. Drobniewski); 1These authors contributed equally to this article.

Main Article

Table 1

Analysis of associations between Mycobacterium tuberculosis phylogenetic lineages defined by SNP analysis and spoligotyping families in the group of isolates not classified using VNTR codes, UK*

Spoligotypes Lineages (6,7) and relevant MIRU codes (12)
M. tuberculosis
M. bovis; 10–2, 40–2, C–5
I/East Asian; 
39–3, A–4, C–4 II/European American; 
16–1,2,3, 39–2, B–1,2 III/EAI; 
23–5, C–2 IV/Indo-Oceanic; 
24–2, 26–2
H37Rv, n = 2 0 2 0 0 0
Beijing, n = 13 13 0 0 0 0
LAM, n = 17 0 17 0 0 0
T, n = 53 1
600740007764671† 51 0 1
777200007403371† 0
Haarlem, n = 21 0 20 0 1
777777774000731† 0
EAI, n = 61 2
477777377413771† 1
777734000000031† 0 58 0
CAS, n = 18 0 0 18 0 0
X, n = 9 0 9 0 0 0
S, n = 2 0 2 0 0 0
Family 33, n = 4 1 1 0 2 0
Family 35, n = 7 7 0 0 0 0
Family 36, n = 5 0 5 0 0 0
M. bovis BCG, n = 4 0 0 0 0 4
M. africanum, n = 35 34 1
710044706302261* 0 0 0

*SNP, single nucleotide polymorphism; VNTR, variable number tandem repeat; MIRU, mycobacterial interspersed repetitive unit; EAI, East African–Indian; LAM Latin American; CAS, Central Asian; BCG, bacillus Calmette-Guérin. European American includes the X, T, LAM, S, and Haarlem families.
†Octal codes indicate spoligotyping patterns for isolates with disagreements between SNP- and spoligotype-defined lineages. Dominant families within each lineage are in boldface.

Main Article

  1. World Health Organization. Global tuberculosis control: surveillance, planning, financing. WHO report 2007 (WHO/HTM/TB/2007.376) [cited 2009 Jul 10].
  2. Sreevatsan  S, Pan  X, Stockbauer  KE, Connell  ND, Kreiswirth  BN, Whittam  TS, Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A. 1997;94:986974. DOIPubMed
  3. Brosch  R, Gordon  SV, Marmiesse  M, Brodin  P, Buchrieser  C, Eiglmeier  K, A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A. 2002;99:36849. DOIPubMed
  4. Alland  D, Lacher  DW, Hazbon  MH, Motiwala  AS, Qi  W, Fleischmann  RD, Role of large sequence polymorphisms (LSPs) in generating genomic diversity among clinical isolates of Mycobacterium tuberculosis and the utility of LSPs in phylogenetic analysis. J Clin Microbiol. 2007;45:3946. DOIPubMed
  5. Gutacker  MM, Mathema  B, Soini  H, Shashkina  E, Kreiswirth  BN, Graviss  EA, Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites. J Infect Dis. 2006;193:1218. DOIPubMed
  6. Gagneux  S, Small  PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis. 2007;7:32837. DOIPubMed
  7. Baker  L, Brown  T, Maiden  MC, Drobniewski  F. Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg Infect Dis. 2004;10:156877.PubMed
  8. Drobniewski  F, Balabanova  Y, Nikolayevsky  V, Ruddy  M, Kuznetzov  S, Zakharova  S, Drug-resistant tuberculosis, clinical virulence, and the dominance of the Beijing strain family in Russia. JAMA. 2005;293:272631. DOIPubMed
  9. Kamerbeek  J, Schouls  L, Kolk  A, van Agterveld  M, van Soolingen  D, Kuijper  S, Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35:90714.PubMed
  10. Vitol  I, Driscoll  J, Kreiswirth  B, Kurepina  N, Bennett  KP. Identifying Mycobacterium tuberculosis complex strain families using spoligotypes. Infect Genet Evol. 2006;6:491504. DOIPubMed
  11. Brudey  K, Driscoll  JR, Rigouts  L, Prodinger  WM, Gori  A, Al-Hajoj  SA, Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol. 2006;6:23. DOIPubMed
  12. Gibson  A, Brown  T, Baker  L, Drobniewski  F. Can 15-locus mycobacterial interspersed repetitive unit-variable-number tandem repeat analysis provide insight into the evolution of Mycobacterium tuberculosis? Appl Environ Microbiol. 2005;71:820713. DOIPubMed
  13. Ferdinand  S, Valetudie  G, Sola  C, Rastogi  N. Data mining of Mycobacterium tuberculosis complex genotyping results using mycobacterial interspersed repetitive units validates the clonal structure of spoligotyping-defined families. Res Microbiol. 2004;155:64754. DOIPubMed
  14. Kremer  K, Au  BK, Yip  PC, Skuce  R, Supply  P, Kam  KM, Use of variable-number tandem-repeat typing to differentiate Mycobacterium tuberculosis Beijing family isolates from Hong Kong and comparison with IS6110 restriction fragment length polymorphism typing and spoligotyping. J Clin Microbiol. 2005;43:31420. DOIPubMed
  15. Gutierrez  MC, Ahmed  N, Willery  E, Narayanan  S, Hasnain  SE, Chauhan  DS, Predominance of ancestral lineages of Mycobacterium tuberculosis in India. Emerg Infect Dis. 2006;12:136774.PubMed
  16. van Deutekom  H, Supply  P, de Haas  PE, Willery  E, Hoijng  SP, Locht  C, Molecular typing of Mycobacterium tuberculosis by mycobacterial interspersed repetitive unit-variable-number tandem repeat analysis, a more accurate method for identifying epidemiological links between patients with tuberculosis. J Clin Microbiol. 2005;43:44739. DOIPubMed
  17. Oelemann  MC, Diel  R, Vatin  V, Haas  W, Rusch-Gerdes  S, Locht  C, Assessment of an optimized mycobacterial interspersed repetitive-unit-variable-number tandem-repeat typing system combined with spoligotyping for population-based molecular epidemiology studies of tuberculosis. J Clin Microbiol. 2007;45:6917. DOIPubMed
  18. Durmaz  R, Zozio  T, Gunal  S, Allix  C, Fauville-Dufaux  M, Rastogi  N. Population-based molecular epidemiological study of tuberculosis in Malatya, Turkey. J Clin Microbiol. 2007;45:402735. DOIPubMed
  19. Anderson  SR, Maguire  H, Carless  J. Tuberculosis in London: a decade and a half of no decline [corrected]. Thorax. 2007;62:1627. DOIPubMed
  20. United Nations. Demographic Yearbook 2000. UN Document ST/ESA/STAT/SER.R/31 2000 [cited 2009 Jul 10].
  21. Collins  CH, Grange  JM, Yates  MD. Tuberculosis bacteriology organization and practice. Oxford (UK): Butterworth-Heinemann; 1997.
  22. Brown  TJ, Herrera-Leon  L, Anthony  RM, Drobniewski  FA. The use of macroarrays for the identification of MDR Mycobacterium tuberculosis. J Microbiol Methods. 2006;65:294300. DOIPubMed
  23. Kwara  A, Schiro  R, Cowan  LS, Hyslop  NE, Wiser  MF, Roahen Harrison  S, Evaluation of the epidemiologic utility of secondary typing methods for differentiation of Mycobacterium tuberculosis isolates. J Clin Microbiol. 2003;41:26835. DOIPubMed
  24. Gopaul  KK, Brown  TJ, Gibson  AL, Yates  MD, Drobniewski  FA. Progression toward an improved DNA amplification-based typing technique in the study of Mycobacterium tuberculosis epidemiology. J Clin Microbiol. 2006;44:24928. DOIPubMed
  25. Nikolayevskyy  V, Gopaul  K, Balabanova  Y, Brown  T, Fedorin  I, Drobniewski  F. Differentiation of tuberculosis strains in a population with mainly Beijing-family strains. Emerg Infect Dis. 2006;12:140613.PubMed
  26. Velji  P, Nikolayevskyy  V, Brown  T, Drobniewski  F. Discriminatory ability of hypervariable variable number tandem repeat loci in population-based analysis of Mycobacterium tuberculosis strains, London, UK. Emerg Infect Dis. 2009;15:160916.PubMed
  27. Allix-Beguec  C, Fauville-Dufaux  M, Supply  P. Three-year population-based evaluation of standardized mycobacterial interspersed repetitive-unit-variable-number tandem-repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2008;46:1398406. DOIPubMed
  28. Hunter  PR, Gaston  MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol. 1988;26:24656.PubMed
  29. New York City Department of Health and Mental Hygiene. 2003 TB Annual Summary [cited 2009 Jul 10].
  30. Che  D, Bitar  D, Desenclos  JC. Epidemiology of tuberculosis in France [in French]. Presse Med. 2006;35:172532. DOIPubMed
  31. Gagneux  S, DeRiemer  K, Van  T, Kato Maeda  M, de Jong  BC, Narayanan  S, Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2006;103:286973. DOIPubMed
  32. Nikolayevskyy  VV, Brown  TJ, Bazhora  YI, Asmolov  AA, Balabanova  YM, Drobniewski  FA. Molecular epidemiology and prevalence of mutations conferring rifampicin and isoniazid resistance in Mycobacterium tuberculosis strains from the southern Ukraine. Clin Microbiol Infect. 2007;13:12938. DOIPubMed
  33. Mathema  B, Kurepina  NE, Bifani  PJ, Kreiswirth  BN. Molecular epidemiology of tuberculosis: current insights. Clin Microbiol Rev. 2006;19:65885. DOIPubMed
  34. Collins  CH, Yates  MD. Mycobacterium africanum and the ‘African’ tubercle bacilli. Med Lab Sci. 1984;41:4103.PubMed
  35. Niemann  S, Kubica  T, Bange  FC, Adjei  O, Browne  EN, Chinbuah  MA, The species Mycobacterium africanum in the light of new molecular markers. J Clin Microbiol. 2004;42:395862. DOIPubMed
  36. Sola  C, Rastogi  N, Gutierrez  MC, Vincent  V, Brosch  R, Parsons  L. Is Mycobacterium africanum subtype II (Uganda I and Uganda II) a genetically well-defined subspecies of the Mycobacterium tuberculosis complex? J Clin Microbiol. 2003;41:13456. DOIPubMed
  37. Caws  M, Thwaites  G, Dunstan  S, Hawn  TR, Lan  NT, Thuong  NT, The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog. 2008;4:e1000034. DOIPubMed
  38. Ruddy  MC, Davies  AP, Yates  MD, Yates  S, Balasegaram  S, Drabu  Y, Outbreak of isoniazid resistant tuberculosis in north London. Thorax. 2004;59:27985. DOIPubMed

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